The evolution of parasite virulence

Pathogens and parasites by definition exert negative effects on the fitness of their hosts. However, they vary in the severity of those effects, such that some diseases allow their hosts to live a long time and suffer few adverse effects, while other hosts are almost instantly overcome and die. Why this variety? Earlier, conventional wisdom led many biologists to believe that parasites would eventually evolve so as not to harm their hosts, on which they depend for their persistence. But in fact the truth, as in the case of HIV (Chapter 8) is often far from this: some parasites evolve to become more virulent over time. So the story must be more complex than the conventional wisdom would suggest.

The major breakthrough in understanding was made by Anderson and May (1982). They derived a general relationship for the fitness of a horizontally transmitted pathogen whose population is at equilibrium with that of its host. In such cases, lifetime reproductive success, R0, is an appropriate measure of fitness:

0 ¡+a + v where P is the transmission rate of the disease, dependent on host density N, a is the parasite induced mortality rate of the host (virulence), v is the host recovery rate, and ¡x is the death rate of uninfected hosts.

If all these parameters are independent of each other, it is clear that virulence should be zero, so as to make R0 as large as possible. This is the sense behind the intuitive, but discredited, conventional wisdom. However, this assumes an absence of genetic correlations between traits. In particular,viru-lence and the transmission rate of the disease might be positively related. One likely source of such a correlation might be that transmission relies on

Fig. 10.1 Virulence and host density. High virulence (black circles) kills off hosts (large circles) rapidly, but that does not matter when hosts are common and the pathogen is easily transmitted (a). However, when hosts are rare, pathogens must be less virulent (fewer black circles) to keep their host alive long enough to encounter susceptible hosts (b).

Fig. 10.1 Virulence and host density. High virulence (black circles) kills off hosts (large circles) rapidly, but that does not matter when hosts are common and the pathogen is easily transmitted (a). However, when hosts are rare, pathogens must be less virulent (fewer black circles) to keep their host alive long enough to encounter susceptible hosts (b).

rapid multiplication of the disease organism within the host to create many disease propagules, or inducing adverse symptoms in the host, such as coughing, that aid transmission. If this is the case, then the optimal virulence for the parasite will be such that the marginal gains of virulence, in terms of added propagule production and transmission, balance the marginal costs, in terms of reduced host survival (Figure 10.1).

The best example of evolution of virulence so as to balance these costs and benefits is that of the rabbit myxoma virus. This virus is endemic to South America but was released into Australia in 1950 to control rabbits. The rabbits had been introduced to Australia by Europeans but had multiplied to plague proportions in the absence of natural predators and disease. On release the myxoma virus did all that had been hoped; it was 99% fatal and reduced rabbit numbers to one-sixth their previous levels in just two years. After just a few years, the effectiveness of the disease had fallen, causing between 70 and 95% fatalities in infected hosts, with a reduction in the effectiveness of control (Fenner and Ratcliffe 1965). It is known that this involved evolution of the virus and not just host evolution or an acquired immunity on the part of the rabbits, because virulence was assessed by exposing the disease to control rabbits from populations that had never encountered the virus.

It is likely that the reduction in virulence seen in the myxoma virus in Australia actually had beneficial effects on transmission rates of the disease. Infected rabbits become weak and immobile and develop skin lesions that aid transmission of the virus to other individuals through mosquito vectors

(Fenner and Ratcliffe 1965). Furthermore, the mosquito vectors are rather seasonal and thus infected hosts must remain alive for extensive periods for the disease to persist. Living infected individuals are thus efficient transmitters of the virus. Although the virus may gain in the short term through more rapid overwhelming of the host, a dead host is no use as a source of transmission.

Hence, selection between hosts infected with strains of the diseases that vary in virulence can cause virulence to evolve to varying levels depending on the strength of the correlations between traits, especially between virulence and transmission rate. There is, however, another potential source of selection on virulence; selection between strains of the disease within a single host. There are two ways in which an individual can acquire more than one strain of a disease. First, an individual can acquire the disease more than once from different sources. An alternative is if the disease mutates and diversifies within the host following a single infection event. Multiple infections can then select for increased virulence. The reason is that now there is competition between unrelated individuals for a single resource. A disease strain that is prudent and is relatively benign to its host will be out-competed by a disease strain that is less prudent but exploits the resource before others can profit from it.

This tendency for a resource shared by unrelated individuals to be overex-ploited is known as the 'tragedy of the commons' (Hardin 1968) and is best known in the context of human overexploitation of marine fisheries. When several individuals exploit a shared host and there is a trade-off between virulence and competitiveness it can be shown that the evolutionary stable virulence strategy is 1 — r (Frank 1996) where r is the average coefficient of relatedness between individuals (Chapter 7). Multiple infections will tend to decrease r and thus increase virulence. HIV infections consist of multiple strains, and should select for increased virulence during the course of an infection and may be the ultimate cause of AIDS onset (Bull 1994).

Therefore, trade-offs between virulence and transmission rates, combined with selection between hosts, and selection within hosts between disease strains can both contribute towards the evolution ofvirulence.A third major variable is known to affect virulence: vertical as opposed to horizontal transmission. If pathogens are vertically transmitted,they are passed from parents to their offspring down the generations. If pathogens are horizontally transmitted they are able to pass between unrelated individuals within a single generation (Figure 10.2). If the proportion of new infections through vertical as opposed to horizontal transmission is high, it pays the pathogen to allow the host to reproduce as much as possible, so that the disease has the opportunity to infect a larger number of host offspring. In this sense the interests of the pathogen and those of the host become more closely aligned

Parent 1

Parent 2

Generation 2 (Offspring)

Generation 1 (Parents)

Parent 1

Parent 2

Generation 2 (Offspring)

Generation 1 (Parents)

Offspring of parent 1 Offspring of parent 2

Fig. 10.2 Horizontal and vertical transmission of parasites (black circles) between hosts (large circles).

Offspring of parent 1 Offspring of parent 2

Fig. 10.2 Horizontal and vertical transmission of parasites (black circles) between hosts (large circles).

through horizontal transmission. Frank (1996) has also showed that a further selective pressure may help reduce the virulence of vertically transmitted pathogen: as transmission becomes more and more exclusively vertical, the chances of multiple infections become very low. Thus, selection for virulence within hosts becomes weaker and weaker.

Is there evidence that vertical transmission selects for benevolence towards hosts? The answer is yes. In a study on fig wasps and their nematode parasites, Herre (1993) found that variation in the opportunity for horizontal as opposed to vertical transmission across species was correlated with the virulence of the nematodes. The wasp species develop in figs that the females must enter in order to lay their eggs. Wasp species differ in the typical number of females that will enter a given fig: sometimes only a single female will enter a fig (the single foundress situation), but at other times many females will enter a single fig (multiple foundresses, see also Chapter 5). After laying her eggs, the female wasp dies inside the fig and her nematodes are released to infect other fig wasps. In the single foundress situation, the nematode parasites of the fig wasp are exclusively transmitted from mother to offspring since there is only one adult wasp per fig. However, if there are multiple foundresses, the nematode progeny can infect the offspring not just of their former host, but those of other wasps, a situation more akin to horizontal transmission. Herre measured the virulence of the nematodes on the wasps by comparing the fecundity of wasps in fig fruits infected with nematodes or free of them. Across 11 species of wasp, he found a positive correlation between the proportion of fruits that were multiple foundress and the virulence of the nematodes. Frank (1996) has since argued that the variation in virulence is most likely caused by changes in the frequency of multiple infection resulting from differences in the mode of transmission, rather than the mode of transmission per se.

So far our discussion of the evolution of antagonism has been restricted to the relative virulence of pathogens and parasites.None of the organisms thus far mentioned are known to have positive fitness effects on their hosts, but vary in the extent of the negative effects they exert. In addition, because we have been focussing on the evolution of parasitic organisms, we have also been concerned exclusively with so-called symbiotic interactions: those that concern long-term associations between the two species relative to the life of one of them. We shall now widen the discussion to include mutualistic relationships including those that do not involve any permanent lifetime association between the two partners.

Waste Management And Control

Waste Management And Control

Get All The Support And Guidance You Need To Be A Success At Understanding Waste Management. This Book Is One Of The Most Valuable Resources In The World When It Comes To The Truth about Environment, Waste and Landfills.

Get My Free Ebook


Post a comment